16.3 Trichomycetes

Microsporidia are fungi that were long thought to be protozoans, and are
still called protozoans by many people who should know better. Trichomycetes, on
the other hand, includes organisms that are clearly protozoans though they were
mistakenly classified as fungi for a long time, and are still called fungi by
many people who should know better.

These extremely common organisms live only in the
digestive tracts of insects and other arthropods, generally as
commensals, sometimes as pathogens or symbionts (mutualists), which are
associated with, although not penetrating, the cuticle lining the digestive
tracts of the host animal. Their hosts include terrestrial, marine and
freshwater arthropods, most commonly midges (Chironomidae), mosquitoes
(Culicidae), black flies (Simuliidae), beetles (Coleoptera), stoneflies
(Plecoptera), and mayflies (Ephemeroptera), as well as several millipedes
(Diplopoda) and crustaceans.

The traditional taxonomy is based on a few micromorphological characters and
the traditional view was to place the class Trichomycetes in the
zygomycetes, the class being divided into four orders:

Amoebidiales (which occur on the external surfaces of freshwater
arthropods),

Asellariales,

Eccrinales, and

Harpellales.

Characteristically the Trichomycetes develop nonseptate (in the Amoebidiales
and Eccrinales) or irregularly septate (in the Harpellales and Asellariales)
vegetative mycelia and asexual sporangia. Further, most genera of the
Harpellales produce zygospores and it is this
character which was used to include all the Trichomycetes among the zygomycete
fungi. The Amoebidiales and the Eccrinales have now been removed from this
association; they are not fungi, but they are close to the
phylogenetically-ancient animal-fungal divergence (Reynolds et al.,
2017).

The Amoebidiales are amoebae-producing organisms that attach to the
exoskeleton of freshwater arthropods (Amoebidium parasiticum was the
first described). Production of amoebae is not otherwise present in kingdom
Fungi. More significantly, A. parasiticum has stacked dictyosomes,
which do not occur in fungi, and lacks chitin in its cell wall. Taken together
these features do not make it a good candidate as a fungus. The Eccrinales have
unbranched, non-septate, multinucleate thalli, and produce sporangiospores,
which form from the apex downward toward the base of the thallus, a feature
found only in kingdom Fungi. These few distinctive morphological characters
together with the fact that they share a very specialised ecological niche with
genuine fungi like the Harpellales was all that classified them within the
Trichomycetes. Now, sequence analyses have
shown that the Eccrinales share a common ancestry with
the Amoebidiales, and are closely related to members of the protist
class Mesomycetozoea, which is positioned at the animal-fungal boundary
in the opisthokont lineage (Mendoza et al., 2002; Cafaro, 2005;
Reynolds et al., 2017).

Removing these fungus-like protists leaves the trichomycetes consisting of
the Harpellales and Asellariales. These are true fungi having hyphal thalli with
cell walls containing chitin fibrils and being regularly septate with incomplete
septa having a plugged central pore. No confirmed sexual stage has been reported
generally for the Asellariales, although conjugation has been reported between
cells of the one species Asellaria ligiae. Generally, in the
Harpellales, though, zygospores (biconical and apically thickened when mature;
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same, or different thalli, being borne at the apex of zygosporophores.
Phylogenetic analyses confirm that the Harpellales and Asellariales both belong
to the subphylum Kickxellomycotina
which is now placed in in phylum
Zoopagomycota (see our earlier discussion in
Section 3.5).

A major difficulty for study of these organisms is that they are
microfungi which are highly specialised for attachment the gut wall of
arthropods and they are obligate endosymbionts; consequently, very few of
them can be cultured axenically (i.e. in pure culture) although this is
needed to prepare fungal macromolecules free of contaminating host
molecules. Only eight of the 38 genera of Harpellales have been cultured,
but none of the Asellariales (Tretter et al., 2014).

The unique trichospores, for which the class is
named, are the asexual spores. Harpellales produce branched or unbranched
thalli, and either the entire thallus or lateral branches of it become
regularly septate at maturity to form a series of uninucleate generative
cells. From the apical region of each generative cell a single unisporous
merosporangium is produced; this is the trichospore (Fig.
3). In many genera the merosporangia are borne on short lateral
branches, which form the collar region of the generative cell. Members of
the Asellariales do not produce deciduous merosporangia but the regularly
septate branches fragment into single-celled arthrospores. In some species
of Asellariales the arthrospores germinate by producing a single branch,
similar in position and form to a trichospore.

Fig. 3. Diagram of the general pattern of asexual reproduction in
Smittium (Harpellales). Redrawn after Moss & Young, 1978.

These insect gut fungi occur worldwide in all habitats;
effectively they have been found whenever they have been looked for. The
Harpellales are predominantly associated with larval aquatic insects, and,
occasionally, with freshwater isopod crustaceans, attached to the midgut or
hindgut linings.

They also attach to the midgut linings of lower dipterans
(Nematocera, which includes mosquitoes, crane flies, black flies, gnats and
midges), mayflies (Ephemeroptera), stoneflies (Plecoptera), beetles (Coleoptera)
and caddisflies (Trichoptera).

The Asellariales includes species that inhabit terrestrial, freshwater and
marine isopods (Isopoda: Crustacea) such as woodlice, pill bugs, and sea
slaters; as well as the hexapod springtails (Collembola) that are primitive
relatives of insects.

They are most often described as being symbiotic with their hosts but the
nature of the association is not at all clear. Certainly, the fungi are highly
specialised for existence within the arthropod guts, so they may be
commensals (an association in which one species derives some benefit
while the other is unaffected). But as fungi they are able to produce many
digestive enzymes so this may be a mutualistic symbiosis in which the fungus
provides nutrients to the insect hosts by assisting with food digestion.
A few species appear to be parasitic at some stage of the host’s development.
All the evidence suggests that only a fraction of the species of arthropod gut
fungi is known.